Host-dependent nitrogen recycling as a mechanism of symbiont control in Aiptasia

Abstract

The metabolic symbiosis with photosynthetic algae allows corals to thrive in the oligotrophic environments of tropical seas. Different aspects of this relationship have been investigated using the emerging model organism Aiptasia. However, many fundamental questions, such as the nature of the symbiotic relationship and the interactions of nutrients between the partners remain highly debated. Using a meta-analysis approach, we identified a core set of 731 high-confidence symbiosis-associated genes that revealed host-dependent recycling of waste ammonium and amino acid synthesis as central processes in this relationship. Subsequent validation via metabolomic analyses confirmed that symbiont-derived carbon enables host recycling of ammonium into nonessential amino acids. We propose that this provides a regulatory mechanism to control symbiont growth through a carbon-dependent negative feedback of nitrogen availability to the symbiont. The dependence of this mechanism on symbiont-derived carbon highlights the susceptibility of this symbiosis to changes in carbon translocation, as imposed by environmental stress.

Author summary

The symbiotic relationship with photosynthetic algae is key to the success of reef building corals in the nutrient poor environment of tropical waters. Extensive insight has been obtained from both physiological and “omics” level studies, yet, there are still gaps in our knowledge with respect to the metabolic interactions in this symbiotic relationship. In particular, the role of the host in nitrogen utilization and its potential link to symbiont population control still remains unclear. Using a meta-analysis approach on publicly available RNA-seq data and isotope-labeled metabolomics, we demonstrate the presence of a negative-feedback cycle in which the host uses symbiont-derived organic carbon to assimilate its own waste ammonium. This host-driven nitrogen recycling process might serve as a molecular mechanism to control symbiont densities in hospite. The dependence of this regulatory mechanism on organic carbon provided by the symbionts explains the sensitivity of this symbiotic relationship to environmental stress.